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Wolbachia action in the sperm produces developmentally deferred chromosome segregation defects during the Drosophila mid-blastula transition

Wolbachia, a vertically transmitted endosymbiont infecting many insects, spreads rapidly through uninfected populations by a mechanism known as cytoplasmic incompatibility (CI). In CI, a paternally delivered modification of the sperm leads to chromatin defects and lethality during and after the firs...

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Autores principales: Warecki, Brandt, Titen, Simon William Abraham, Alam, Mohammad Shahriyar, Vega, Giovanni, Lemseffer, Nassim, Hug, Karen, Minden, Jonathan S, Sullivan, William
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9507124/
https://www.ncbi.nlm.nih.gov/pubmed/36149408
http://dx.doi.org/10.7554/eLife.81292
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author Warecki, Brandt
Titen, Simon William Abraham
Alam, Mohammad Shahriyar
Vega, Giovanni
Lemseffer, Nassim
Hug, Karen
Minden, Jonathan S
Sullivan, William
author_facet Warecki, Brandt
Titen, Simon William Abraham
Alam, Mohammad Shahriyar
Vega, Giovanni
Lemseffer, Nassim
Hug, Karen
Minden, Jonathan S
Sullivan, William
author_sort Warecki, Brandt
collection PubMed
description Wolbachia, a vertically transmitted endosymbiont infecting many insects, spreads rapidly through uninfected populations by a mechanism known as cytoplasmic incompatibility (CI). In CI, a paternally delivered modification of the sperm leads to chromatin defects and lethality during and after the first mitosis of embryonic development in multiple species. However, whether CI-induced defects in later stage embryos are a consequence of the first division errors or caused by independent defects remains unresolved. To address this question, we focused on ~1/3 of embryos from CI crosses in Drosophila simulans that develop apparently normally through the first and subsequent pre-blastoderm divisions before exhibiting mitotic errors during the mid-blastula transition and gastrulation. We performed single embryo PCR and whole genome sequencing to find a large percentage of these developed CI-derived embryos bypass the first division defect. Using fluorescence in situ hybridization, we find increased chromosome segregation errors in gastrulating CI-derived embryos that had avoided the first division defect. Thus, Wolbachia action in the sperm induces developmentally deferred defects that are not a consequence of the first division errors. Like the immediate defect, the delayed defect is rescued through crosses to infected females. These studies inform current models on the molecular and cellular basis of CI.
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spelling pubmed-95071242022-09-24 Wolbachia action in the sperm produces developmentally deferred chromosome segregation defects during the Drosophila mid-blastula transition Warecki, Brandt Titen, Simon William Abraham Alam, Mohammad Shahriyar Vega, Giovanni Lemseffer, Nassim Hug, Karen Minden, Jonathan S Sullivan, William eLife Cell Biology Wolbachia, a vertically transmitted endosymbiont infecting many insects, spreads rapidly through uninfected populations by a mechanism known as cytoplasmic incompatibility (CI). In CI, a paternally delivered modification of the sperm leads to chromatin defects and lethality during and after the first mitosis of embryonic development in multiple species. However, whether CI-induced defects in later stage embryos are a consequence of the first division errors or caused by independent defects remains unresolved. To address this question, we focused on ~1/3 of embryos from CI crosses in Drosophila simulans that develop apparently normally through the first and subsequent pre-blastoderm divisions before exhibiting mitotic errors during the mid-blastula transition and gastrulation. We performed single embryo PCR and whole genome sequencing to find a large percentage of these developed CI-derived embryos bypass the first division defect. Using fluorescence in situ hybridization, we find increased chromosome segregation errors in gastrulating CI-derived embryos that had avoided the first division defect. Thus, Wolbachia action in the sperm induces developmentally deferred defects that are not a consequence of the first division errors. Like the immediate defect, the delayed defect is rescued through crosses to infected females. These studies inform current models on the molecular and cellular basis of CI. eLife Sciences Publications, Ltd 2022-09-23 /pmc/articles/PMC9507124/ /pubmed/36149408 http://dx.doi.org/10.7554/eLife.81292 Text en © 2022, Warecki, Titen et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Warecki, Brandt
Titen, Simon William Abraham
Alam, Mohammad Shahriyar
Vega, Giovanni
Lemseffer, Nassim
Hug, Karen
Minden, Jonathan S
Sullivan, William
Wolbachia action in the sperm produces developmentally deferred chromosome segregation defects during the Drosophila mid-blastula transition
title Wolbachia action in the sperm produces developmentally deferred chromosome segregation defects during the Drosophila mid-blastula transition
title_full Wolbachia action in the sperm produces developmentally deferred chromosome segregation defects during the Drosophila mid-blastula transition
title_fullStr Wolbachia action in the sperm produces developmentally deferred chromosome segregation defects during the Drosophila mid-blastula transition
title_full_unstemmed Wolbachia action in the sperm produces developmentally deferred chromosome segregation defects during the Drosophila mid-blastula transition
title_short Wolbachia action in the sperm produces developmentally deferred chromosome segregation defects during the Drosophila mid-blastula transition
title_sort wolbachia action in the sperm produces developmentally deferred chromosome segregation defects during the drosophila mid-blastula transition
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9507124/
https://www.ncbi.nlm.nih.gov/pubmed/36149408
http://dx.doi.org/10.7554/eLife.81292
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